Bottom Line:
We predicted that starlings from larger broods, specifically those that had experienced more nest competitors larger than themselves would exhibit reduced expectation of reward, indicative of a 'pessimistic', depression-like mood.Thus, increased competition in the nest and poor current somatic state appear to have opposite effects on cognitive biases.Our results lead us to question whether increased expectation of reward when presented with ambiguous stimuli always indicates a more positive affective state.

ABSTRACTMoods are enduring affective states that we hypothesise should be affected by an individual's developmental experience and its current somatic state. We tested whether early-life adversity, induced by manipulating brood size, subsequently altered juvenile European starlings' (Sturnus vulgaris) decisions in a judgment bias task designed to provide a cognitive measure of mood. We predicted that starlings from larger broods, specifically those that had experienced more nest competitors larger than themselves would exhibit reduced expectation of reward, indicative of a 'pessimistic', depression-like mood. We used a go/no-go task, in which 30 starlings were trained to probe a grey card disc associated with a palatable mealworm hidden underneath and avoid a different shade of grey card disc associated with a noxious quinine-injected mealworm hidden underneath. Birds' response latencies to the trained stimuli and also to novel, ambiguous stimuli intermediate between these were subsequently tested. Birds that had experienced greater competition in the nest were faster to probe trained stimuli, and it was therefore necessary to control statistically for this difference in subsequent analyses of the birds' responses to the ambiguous stimuli. As predicted, birds with more, larger nest competitors showed relatively longer latencies to probe ambiguous stimuli, suggesting reduced expectation of reward and a 'pessimistic', depression-like mood. However, birds with greater developmental telomere attrition--a measure of cellular aging associated with increased morbidity and reduced life-expectancy that we argue could be used as a measure of somatic state--showed shorter latencies to probe ambiguous stimuli. This would usually be interpreted as evidence for a more positive or 'optimistic' affective state. Thus, increased competition in the nest and poor current somatic state appear to have opposite effects on cognitive biases. Our results lead us to question whether increased expectation of reward when presented with ambiguous stimuli always indicates a more positive affective state. We discuss the possibility that birds in poor current somatic state may adopt a 'hungry' cognitive phenotype that could drive behaviour commonly interpreted as 'optimism' in food-rewarded cognitive bias tasks.

pone.0132602.g003: Effects of genetic family on judgment bias.Latency to probe as a function of stimulus valence for each of the 8 genetic families. Families FH6 and P11 contained 3 birds and the other families contained 4 birds. Data are mean ± 1 s.e. latency to probe in the judgment bias test trials. The dotted lines show the mean speed for each family (the mean of the mean latencies to probe POS and NEG). The top row of families were ‘pessimists’, meaning that their mean latencies to probe ambiguous stimuli were predominantly greater than the mean speed and more similar to NEG, whereas the bottom row were ‘optimists’, meaning that their mean latencies to probe ambiguous stimuli were predominantly less than the mean speed and more similar to POS.

Mentions:
In all preceding analyses we included genetic family as a random effect because we assumed that birds from the same family were likely to be more similar to each other than birds chosen at random, but this assumption was not tested explicitly. Fig 3 shows the cognitive bias data split by family. To test whether mean speed differed between families, we fitted a model with speed as the dependent variable and family as a random effect. Family explained none of the variance in speed, and there was no significant change in deviance when family was dropped from the model (GLMM: X2(1) = 0.00, p = 1.000). To test whether responses to ambiguous stimuli in particular differed between families, we fitted a model with latency to probe (logged) as the dependent variable, speed and valence (2–4) as fixed predictors and family and bird as nested random effects. Genetic family explained 6.4% of the variance and there was a significant change in deviance when family was dropped from the model (Χ2(1) = 4.78, p = 0.029), suggesting a significant effect of genetic family.

pone.0132602.g003: Effects of genetic family on judgment bias.Latency to probe as a function of stimulus valence for each of the 8 genetic families. Families FH6 and P11 contained 3 birds and the other families contained 4 birds. Data are mean ± 1 s.e. latency to probe in the judgment bias test trials. The dotted lines show the mean speed for each family (the mean of the mean latencies to probe POS and NEG). The top row of families were ‘pessimists’, meaning that their mean latencies to probe ambiguous stimuli were predominantly greater than the mean speed and more similar to NEG, whereas the bottom row were ‘optimists’, meaning that their mean latencies to probe ambiguous stimuli were predominantly less than the mean speed and more similar to POS.

Mentions:
In all preceding analyses we included genetic family as a random effect because we assumed that birds from the same family were likely to be more similar to each other than birds chosen at random, but this assumption was not tested explicitly. Fig 3 shows the cognitive bias data split by family. To test whether mean speed differed between families, we fitted a model with speed as the dependent variable and family as a random effect. Family explained none of the variance in speed, and there was no significant change in deviance when family was dropped from the model (GLMM: X2(1) = 0.00, p = 1.000). To test whether responses to ambiguous stimuli in particular differed between families, we fitted a model with latency to probe (logged) as the dependent variable, speed and valence (2–4) as fixed predictors and family and bird as nested random effects. Genetic family explained 6.4% of the variance and there was a significant change in deviance when family was dropped from the model (Χ2(1) = 4.78, p = 0.029), suggesting a significant effect of genetic family.

Bottom Line:
We predicted that starlings from larger broods, specifically those that had experienced more nest competitors larger than themselves would exhibit reduced expectation of reward, indicative of a 'pessimistic', depression-like mood.Thus, increased competition in the nest and poor current somatic state appear to have opposite effects on cognitive biases.Our results lead us to question whether increased expectation of reward when presented with ambiguous stimuli always indicates a more positive affective state.

ABSTRACTMoods are enduring affective states that we hypothesise should be affected by an individual's developmental experience and its current somatic state. We tested whether early-life adversity, induced by manipulating brood size, subsequently altered juvenile European starlings' (Sturnus vulgaris) decisions in a judgment bias task designed to provide a cognitive measure of mood. We predicted that starlings from larger broods, specifically those that had experienced more nest competitors larger than themselves would exhibit reduced expectation of reward, indicative of a 'pessimistic', depression-like mood. We used a go/no-go task, in which 30 starlings were trained to probe a grey card disc associated with a palatable mealworm hidden underneath and avoid a different shade of grey card disc associated with a noxious quinine-injected mealworm hidden underneath. Birds' response latencies to the trained stimuli and also to novel, ambiguous stimuli intermediate between these were subsequently tested. Birds that had experienced greater competition in the nest were faster to probe trained stimuli, and it was therefore necessary to control statistically for this difference in subsequent analyses of the birds' responses to the ambiguous stimuli. As predicted, birds with more, larger nest competitors showed relatively longer latencies to probe ambiguous stimuli, suggesting reduced expectation of reward and a 'pessimistic', depression-like mood. However, birds with greater developmental telomere attrition--a measure of cellular aging associated with increased morbidity and reduced life-expectancy that we argue could be used as a measure of somatic state--showed shorter latencies to probe ambiguous stimuli. This would usually be interpreted as evidence for a more positive or 'optimistic' affective state. Thus, increased competition in the nest and poor current somatic state appear to have opposite effects on cognitive biases. Our results lead us to question whether increased expectation of reward when presented with ambiguous stimuli always indicates a more positive affective state. We discuss the possibility that birds in poor current somatic state may adopt a 'hungry' cognitive phenotype that could drive behaviour commonly interpreted as 'optimism' in food-rewarded cognitive bias tasks.